Abstract

Individual recognition is thought to be a crucial ability facilitating the evolution of animal societies. Given its central importance, much research has addressed the extent of this capacity across the animal kingdom. Recognition of individuals vocally has received particular attention due, in part, to the insights it provides regarding the cognitive processes that underlie this skill. While much work has focused on vocal individual recognition in primates, there is currently very little data showing comparable skills in non-primate mammals under natural conditions. This may be because non-primate mammal societies do not provide obvious contexts in which vocal individual recognition can be rigorously tested. We addressed this gap in understanding by designing an experimental paradigm to test for individual recognition in meerkats (Suricata suricatta) without having to rely on naturally occurring social contexts. Results suggest that when confronted with a physically impossible scenario—the presence of the same conspecific meerkat in two different places—subjects responded more strongly than during the control, a physically possible setup. We argue that this provides the first clear evidence for vocal individual recognition in wild non-primate mammals and hope that this novel experimental design will allow more systematic cross-species comparisons of individual recognition under natural settings.

1. Introduction

Individual recognition of conspecifics is considered to be crucial to the evolution of animal sociality [1,2]. Given its central importance, much research has addressed the competence of various animal species in this behavioural and cognitive domain [3]. Owing to their rich and multi-faceted social lives, primates have received particular attention, with numerous studies demonstrating intra-group individual recognition through the playback of vocalizations (see [4]). Evidence for equivalent abilities in wild non-primates is much less clear for two reasons: (i) it has proven difficult to find socially meaningful contexts where individual vocal identification would be more advantageous than class-level vocal recognition, other than mother–infant interactions [5,6], and (ii) social and ecological differences make it hard to find a good experimental framework for cross-species comparisons [7]. We addressed these issues by devising a novel violation-of-expectation paradigm favouring individual recognition in meerkats (Suricata suricatta), but which does not depend on naturally occurring social interactions.

Meerkats, like primates, rely heavily on vocal communication to coordinate their activities according to their surrounding ecological situation, such as the risk of predation [8]. However, exactly how important vocalizations are for tracking changes in their social environment is currently not clear [9]. During social foraging, meerkats frequently emit stereotyped, individually distinctive, ‘close calls’, which most likely function in maintaining group cohesion [10]. Using a dual-speaker setup, we simulated two physical scenarios: (i) incongruent (test) condition: the same subordinate meerkat foraging on one side of the subject and then within a few seconds (physically impossible) appearing on the geometrically opposite side; and (ii) congruent (control) condition: two subordinates foraging independently on either side of the subject. If meerkats use vocalizations to recognize and track conspecific group members individually, we predicted they should respond more during the incongruent, physically impossible condition, in terms of vigilance behaviour and looking in the direction of the expectancy violation (loudspeaker from which the second playback was broadcast), than during the socially and physically congruent condition.

2. Methods

(a) Study site and subjects

Recordings and playback experiments were conducted on wild but habituated meerkats at the Kalahari Meerkat Project, South Africa [8], between October and December 2010 (see the electronic supplementary material).

(b) Call recording and playback construction

We recorded close calls from male subordinate meerkats (more than 12 months) belonging to the same group as playback subjects at a distance of approximately 1–2 m, using a Sennheiser directional microphone (ME66/K6) connected to a Marantz PMD-670 solid-state recorder. In one group, subordinate females were recorded and used as playback stimuli, as no males in this group were habituated to a sufficient level to allow good quality call collection. Calls were transferred digitally onto a PC using Cool Edit Pro 2000. Up to six foraging close calls with a high signal-to-noise ratio were selected randomly from sound files and used to construct playbacks. In the test and control conditions, two independent playbacks of 4.5 s consisting of between two and three close calls were created (see the electronic supplementary material). In the test (incongruent) condition, the two playback files consisted of different close calls recorded from the same individual. In the control (congruent) condition, one playback file consisted of close calls from the same subordinate group member as used in the test condition and in the second playback file, close calls from a different subordinate meerkat.

(c) Playback protocol

Playback experiments were conducted on eight male subordinate meerkats belonging to eight different groups. All subjects were followed while foraging for a minimum of 30 min (range 0.5–2.5 h) prior to playback. While the subject was foraging, both experimenters attached a loudspeaker (model: JBL on tour) to their legs at a height similar to that of another foraging meerkat and positioned themselves at geometrically opposite sides of the subject. Experimenter one was approximately 2 m from the subject to allow accurate filming at a close distance, while experimenter two was approximately 5 m from the subject and 7 m from experimenter 1 (figure 1). The experimental setup was kept exactly the same in both test and control conditions so as to rule out any distance-based effects owing to asymmetrical speaker placement, which might otherwise explain subjects' response. Keeping track of the spatial position of the two subordinates used as stimuli (to ensure spatial congruency), we then played back from an iPod touch either different calls from the same individual from both sides (test condition), or calls from two different individuals from both sides (control condition), with an approximately 4 s interval between stimuli. In the test condition, we therefore simulated an incongruent situation; that a subordinate individual was relaxed and foraging on one side of the subject and then a few seconds later appears on the opposite side 7 m from its original position, again in a relaxed social foraging state. By presenting subjects with different calls from the same individual, we ensure that any violation of expectation response in the incongruent condition would be based on the listener's recognition that the calls came from the same individual, not that they constituted the exact same stimulus. In the control condition, we simulated a congruent scenario: the presence of two relaxed independently foraging meerkats on opposite sides of the subject. Subjects were filmed for 30 s prior to the beginning of the first playback and 1 min after the end of the second playback. To avoid order effects, we randomized the order in which subjects heard test and control conditions.

Schematic outlining the playback protocol used in both the (a) incongruent (test) and (b) congruent (control) conditions.

(d) Behavioural responses

We analysed videos frame-by-frame using iMovie (MAC OS, 2010). Because we were playing back close calls, a frequently produced, low-arousal state vocalization, and because the situation we were simulating was not socially significant in comparison with previous vocal individual recognition studies [11], we did not expect overt behavioural responses to the violation-of-expectation setup. We therefore primarily focused on the employment of vigilance behaviour, a common alert-related behaviour which meerkats are known to demonstrate during socially or ecologically important events [10], for the duration of the second playback plus a 5 s time window following the final call played back. This time window was specifically chosen to compensate for possible responses to the final call played back and because all subjects had already returned to relaxed foraging by this time. The first playbacks in both the test and control conditions were used to assess baseline vigilance behaviour (see the electronic supplementary material). We noted: (i) each time the subject was observed to scan the surrounding terrestrial area; (ii) the duration of each vigilance bout, defined as the frame at which the meerkat began vigilance after having previously held its head in a different position to the frame at which the meerkat returned its head to a foraging posture; and (iii) if vigilance performed was in the direction of the speaker from which the second playback was broadcast. To ensure accurate coding of videotapes a second observer blind-coded 50 per cent of trials (see electronic supplementary material, 8 videos).

(e) Statistical analysis

Owing to the non-normal nature of the data and the small sample size, we employed exact non-parametric tests ([12]; see the electronic supplementary material).

4. Discussion

Although vocal individual recognition is assumed to be widespread among non-primate animals, clear experimental evidence obtained under natural settings is surprisingly elusive. The lack of evidence is most probably owing to the difficulty of empirically testing between individual recognition and categorization based on social status [3]. Our results suggest that when confronted with an impossible socio-physical scenario—the presence of the same individual on two different sides—meerkats are more vigilant and more likely to look in the direction of the expectancy violation than when the presence of two different individuals is simulated. In both conditions, subordinates from within the same group were used as subjects and playback stimuli; this allows us to rebut the common argument that discrimination occurs only at the more rudimentary class or group level, leading us to conclude that meerkats distinguish between individuals.

Meerkats live in stable, cooperatively breeding social groups of up to 50 individuals [13]. Individuals are continually exposed to a number of social challenges, including aggression, competition for dominance and coordination of cooperative behaviours [14]. Keeping track of conspecifics with whom individuals have differentiated competitive and cooperative relations is therefore a crucial requirement for the successful maintenance of meerkat social systems. Commonly emitted close calls, indicating the position and identity of the caller, may be one medium through which this occurs.

A recent study at the same site has shown that subordinate female meerkats can recognize the dominant female vocally [15]; however, given that there is only ever one dominant female in each group, that study could not logically show that this goes beyond category-level recognition of dominant females. In the present study, we have shown within-class discrimination of subordinate individuals who are tracked spatially. Hence, we suggest that meerkats do indeed have a concept of conspecifics as ‘individuals’ recognized perceptually. Exactly what cognitive mechanisms underlie this discrimination is not clear. For example, this experiment does not allow us to determine whether or not meerkats form a global representation of individuals by integrating identity cues from multiple modalities [16]. The absence of experimental evidence for multiple modality integration does not necessarily negate the presence of individual recognition through auditory cues alone. Humans recognize the voices of radio personalities they have never seen, and recent work in auditory perception suggests that short-term memory in hearing is based on auditory objects that bind related elements of the auditory scene into a single representation [17].

Understanding how animals experience the individuals within their social worlds is key to deciphering the evolution of social and communicative capacities as sophisticated as those in humans [18]. Our results, indicating individual recognition in a non-primate mammal under natural conditions, highlight the possibility that the task of monitoring the location of group members based on their vocalizations may employ recognition mechanisms similar to those demonstrated in more complex social interactions, such as third-party relationships, or coalition formations. We hope our results will encourage others to employ similar violation-of-expectancy experimental paradigms when natural social contexts in which to test individual recognition are lacking. This may ultimately allow more systematic cross-species comparison of individual recognition.

Acknowledgements

Thanks to Tim Clutton-Brock for research permission, Elizabeth Wiley for help with experiments, Leanne Proops for discussions, Brian Scholl for expert advice, and Robert Seyfarth and an anonymous reviewer for helpful comments on the manuscript. Funding to S.W.T. and M.B.M. was provided by Zurich University, and to C.A. by the Alexander von Humboldt Foundation and Indiana University.

2006In a songbird, the black redstart, parents use acoustic cues to discriminate between their different fledglings. Anim. Behav.71, 1039–1046.doi:10.1016/j.anbehav.2005.06.022 (doi:10.1016/j.anbehav.2005.06.022)